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A Revision of Pipistrelle-Like Bats (Mammalia: Chiroptera: Vespertilionidae) in East Africa with the Description of New Genera and Species

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A Revision of Pipistrelle-Like Bats (Mammalia: Chiroptera: Vespertilionidae) in East Africa with the Description of New Genera and Species applyparastyle “fig//caption/p[1]” parastyle “FigCapt” Zoological Journal of the Linnean Society, 2020, XX, 1–33. With 10 figures. Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlaa087/5903787 by University of New England user on 10 September 2020 A revision of pipistrelle-like bats (Mammalia: Chiroptera: Vespertilionidae) in East Africa with the description of new genera and species ARA MONADJEM1,2,3, , TERRENCE C. DEMOS3, DESIRE L. DALTON1,4, PAUL W. WEBALA5, SIMON MUSILA6, JULIAN C. KERBIS PETERHANS3,7 and BRUCE D. PATTERSON3 1Department of Biological Sciences, University of Eswatini, Private Bag 4, Kwaluseni, Eswatini 2Mammal Research Institute, Department of Zoology and Entomology, University of Pretoria, Private Bag 20, Hatfield 0028, Pretoria, South Africa 3Negaunee Integrative Research Center, Field Museum of Natural History, Chicago, IL 60605, USA 4South African National Biodiversity Institute, PO Box 754, Pretoria 0001, South Africa 5Department of Forestry and Wildlife Management, Maasai Mara University, Narok 20500, Kenya 6Mammalogy Section, Zoology Department, National Museums of Kenya, PO Box 40658-00100, Nairobi, Kenya 7College of Arts & Sciences, Roosevelt University, 430 S Michigan, Chicago, IL 60605, USA Received 29 May 2020; revised 1 July 2020; accepted for publication 4 July 2020 Vespertilionidae (class Mammalia) constitutes the largest family of bats, with ~500 described species. Nonetheless, the systematic relationships within this family are poorly known, especially among the pipistrelle-like bats of the tribes Vespertilionini and Pipistrellini. Perhaps as a result of their drab pelage and lack of obvious morphological characters, the genus and species limits of pipistrelle-like bats remain poorly resolved, particularly in Africa, where more than one-fifth of all vesper bat species occur. Further exacerbating the problem is the accelerating description of new species within these groups. In this study, we attempt to resolve the systematic relationships among the pipistrelle-like bats of sub-Saharan Africa and Madagascar and provide a more stable framework for future systematic efforts. Our systematic inferences are based on extensive genetic and morphological sampling of > 400 individuals covering all named genera and the majority of described African pipistrelle-like bat species, focusing on previously unstudied samples of East African bats. Our study corroborates previous work by identifying three African genera in Pipistrellini (Pipistrellus, Scotoecus and Vansonia), none of which is endemic to Africa. However, the situation is more complex in Vespertilionini. With broad taxonomic sampling, we confirm that the genus Neoromicia is paraphyletic, a situation that we resolve by assigning the species of Neoromicia to four genera. Neoromicia is here restricted to Neoromicia zuluensis and allied taxa. Some erstwhile Neoromicia species are transferred into an expanded Laephotis, which now includes both long- eared and short-eared forms. We also erect two new genera, one comprising a group of mostly forest-associated species (many of which have white wings) and the other for the genetically and morphologically unique banana bat. All four of these genera, as recognized here, are genetically distinct, have distinctive bacular morphologies and can be grouped by cranial morphometrics. We also demonstrate that the genus Nycticeinops, until now considered monospecific, includes both Afropipistrellus and the recently named Parahypsugo, thus representing the fifth African genus in Vespertilionini. A sixth genus, Hypsugo, is mostly extra-limital to sub-Saharan Africa. Finally, we describe three new species of pipistrelle-like bats from Kenya and Uganda, uncovered during the course of systematic bat surveys in the region. Such surveys are greatly needed across tropical Africa to uncover further bat diversity. ADDITIONAL KEYWORDS: Africa – alpha taxonomy – genus revision – Mammalia – mitochondrial DNA – new genera – new species. *Corresponding author. E-mail: [email protected] [Version of record, published online 10 September 2020; http:// zoobank.org/ urn:lsid:zoobank.org:pub: 71737F08-2938-4403- 8385-5438B2E5EABE] © 2020 The Linnean Society of London, Zoological Journal of the Linnean Society, 2020, XX, 1–33 1 2 A. MONADJEM ET AL. INTRODUCTION attention (Monadjem et al., 2020b). Previous studies have suggested that it might be paraphyletic (Koubínová Downloaded from https://academic.oup.com/zoolinnean/advance-article/doi/10.1093/zoolinnean/zlaa087/5903787 by University of New England user on 10 September 2020 Vespertilionidae is the largest chiropteran family et al., 2013; Monadjem et al., 2013; Goodman et al., in the world, with ~500 described species in 54 2015), and a close relationship between the distinctly genera (Moratelli & Burgin, 2019), of which 17 long-eared Laephotis Thomas, 1901 species and some genera and ≥ 106 species have been reported from members of the genus Neoromicia has been reported Africa (AfricanBats NPC, 2019; Monadjem et al., (Hoofer & Van den Bussche, 2003; Görföl & Csorba, 2020b). Within this group, the taxonomy of the 2018). Furthermore, the placement of Neoromicia nana pipistrelle-like or ‘pipistrelloid’ tribes Pipistrellini (Peters, 1852) (sometimes previously called Pipistrellus and Vespertilionini (sensu Amador et al., 2018), nanus or Hypsugo nanus) has been problematic. For subfamily Vespertilioninae, has been particularly example, unlike other species placed in Neoromicia, difficult to resolve. The systematic relationships of Neo. nana has a distinctive character set: the first these bats have been the subject of much debate over upper premolar is present, the braincase is obviously the past few decades (Hill & Harrison, 1987; Volleth and highly inflated, there is a distinct thumbpad & Heller, 1994; Hoofer & Van den Bussche, 2003; present at the base of the thumb, and the lower third Roehrs, Lack & Van den Bussche, 2010; Koubínová molar is ‘nyctalodont’ (Monadjem et al., 2010; Van et al., 2013; Amador et al., 2018; Moratelli & Burgin, Cakenberghe & Happold, 2013). Another taxonomic 2019). A well-supported phylogeny, particularly problem relates to the newly described Afrotropical of basal nodes, has not yet been published, and genus Parahypsugo, which is rendered paraphyletic by although species limits are poorly known for many Pipistrellus (Afropipistrellus) grandidieri Dobson, 1876 taxa (Andriollo et al., 2015), new species and genera (Monadjem et al., 2020a), and the relationship of these continue to be described (Benda et al., 2016; Hutterer two groups has not yet been investigated with respect to et al., 2019; Görföl et al., 2020). Nycticeinops Hill & Harrison, 1987. The high diversity of pipistrelle-like bats in Africa In contrast, the systematic relationships in has been overshadowed by the ambiguity of species Pipistrellini are somewhat more clear (Hoofer & relationships and further complicated by the local or Van den Bussche, 2003; Amador et al., 2018). Sub- regional focus of previous analyses (Monadjem et al., Saharan Africa was previously thought to be home to 2013; Goodman et al., 2015, 2017; Hutterer et al., 2019). two genera, Pipistrellus and Scotoecus Thomas, 1901. For example, in the past decade, two new species have However, a recent study demonstrated that Pipistrellus been described in the genus Neoromicia Roberts, 1926 rueppellii J. Fischer, 1829 is sister to Pipistrellus (Monadjem et al., 2013; Decher et al., 2015), a third + Nyctalus + Glischropus (Koubínová et al., 2013), in Pipistrellus Kaup, 1829 (Monadjem et al., 2020a) rendering that concept of Pipistrellus paraphyletic. and a fourth in Parahypsugo Hutterer et al., 2019, all Based on this evidence and the distinctive morphology from the Upper Guinea forest zone of West Africa. The of Pip. rueppellii, this species has since been placed phylogenetic relationships of pipistrelle-like bats in this in its own genus, Vansonia (Roberts, 1946), which region have been investigated with mitochondrial DNA was formerly recognized as a subgenus of Pipistrellus markers, and a new genus (Parahypsugo) was recognized (Moratelli & Burgin, 2019). New species continue to be based on genetic and morphological characters (Hutterer described in this tribe (Monadjem et al., 2020a). & Kerbis Peterhans, 2019; Monadjem et al., 2020a). The main objectives of this study are as follows: (1) to Likewise, the species identities and relationships present a phylogeny for pipistrelle-like vespertilionids of pipistrelle-like bats in Madagascar have been (tribes Pipistrellini and Vespertilionini) in sub- re-examined (Goodman & Ranivo, 2004; Bates et al., Saharan Africa based on a unique dataset of > 400 2006; Goodman et al., 2012, 2015), as have the southern specimens that have been sequenced and examined African Neoromicia (Goodman et al., 2017). In contrast, morphologically; (2) to investigate the putative the pipistrelle-like bats of East Africa have received paraphyly within the genus Neoromicia and resolve almost no attention, and many basic taxonomic and this taxonomic problem; and (3) to use an integrative systematic questions remain unanswered (Patterson & taxonomic approach to describe three East African Webala, 2012). East Africa appears to be a hub of cryptic species new to science. diversity in other bat families and genera (Demos et al., 2018, 2019a, b, 2020; Patterson et al., 2018, 2019, 2020). Mizerovská et al. (2019) argued that this is true for non- volant mammal faunas, and we
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